Download Wooded habitat edges as refugia from microtine herbivory in

OIKOS 100: 525–533, 2003
Wooded habitat edges as refugia from microtine herbivory in
tallgrass prairies
Anne M. Nickel, Brent J. Danielson and Kirk A. Moloney
Nickel, A. M., Danielson, B. J. and Moloney, K. A. 2003. Wooded habitat edges as
refugia from microtine herbivory in tallgrass prairies. – Oikos 100: 525– 533.
Meadow voles, Microtus pennsyl6anicus, affect the species composition, distribution,
and succession of plants in grassland ecosystems, but the effects of voles on
herbaceous plants when grasslands are bordered by wooded edges is not known. We
investigated the impact of wooded edges on vole distribution and herbivory of
relatively palatable and unpalatable native prairie plant species by studying five
reconstructed tallgrass prairies with wooded edges in central Iowa. A 50 × 50 m
trapping grid at each site was established to determine the proportion of voles
captured at various distances from the edge. We found that meadow voles were less
abundant at wooded edges and, in general, increased in number toward the prairie
interior. Seedlings of purple prairie clover (Dalea purpurea) and Illinois bundleflower
(Desmanthus illinoensis), a relatively palatable and unpalatable species, respectively,
were transplanted onto simulated gopher mounds 2, 5, 10, 20 and 30 m from the
edge. The number of plants grazed per species per mound was determined 1 week and
4 weeks after planting. The amount of herbivory on both species was significantly
different by distance, with fewer plants eaten 2 m from the edge. Interestingly, the
amount of herbivory on relatively unpalatable plants did not differ from more
palatable plants. Herbivory on both plant species also varied by site, such that sites
with lower vole density tended to have lower amounts of herbivory. These results
indicate that wooded edges do have an effect on meadow vole distribution and native
prairie seedling herbivory. Because voles avoid wooded edges, seedlings of any species
may experience a small refuge from herbivory along wooded edges.
A. M. Nickel, B. J. Danielson and K. A. Moloney, Ecology and E6olutionary Biology
Interdisciplinary Graduate Program, 353 Bessey Hall, Iowa State Uni6., Ames, IA
50011, USA ([email protected]).
In Iowa, restoration and reconstruction of native
prairie has been on the rise in the last decade as
awareness of the importance of this ecosystem and need
for recovery has grown (Smith 1998). Agricultural fields
and roadsides are being reclaimed and planted with
native vegetation throughout the Great Plains. Because
of the fragmented nature of prairie remnants and reconstructions, prairies often border the wooded edges
of agricultural fields and riparian corridors. Habitat
edges can influence critical ecological mechanisms, patterns, and dynamics at a variety of spatial scales (Fagan
et al. 1999). For example, small mammals are known to
be sensitive to edges, and because they are frequently
abundant, they may cause spatial structuring of the
plant community. In particular, the wooded edges of
prairies may affect the abundance and distribution of
small mammals inhabiting prairies, and consequently
affect the survival of forage species.
Small mammals play an important role in prairie
ecosystems. According to Kaufman and Kaufman
(1997), small mammals may modify, maintain, or create
habitat conditions through grazing, granivory, dispersal
of seeds, and disturbance of prairie vegetation. Thus,
by affecting the behavior and local abundance of small
mammals, edges may significantly alter the species composition, distribution, succession, and ultimately the
function of prairie ecosystems. Few studies have investigated the effects of edges on species of mammals occur-
Accepted 27 August 2002
Copyright © OIKOS 2003
ISSN 0030-1299
OIKOS 100:3 (2003)
525
ring in native or reconstructed prairies (but see Ostfeld
et al. 1997, Patitschniak-Arts and Messier 1998, Manson et al. 1999, and Manson et al. 2001 for studies in
old fields). As the number of small-scale prairie reconstructions and the desire for them to function as a
native prairie increases, the study of edge effects on
prairie small-mammal and plant communities becomes
more crucial.
One small mammal, the meadow vole (Microtus
pennsyl6anicus), is of particular interest for edge studies
because of its high abundance and widespread distribution. Meadow voles are the dominant small-mammal
species in herbaceous habitats of eastern North America (Ostfeld and Manson 1996), and throughout the
tallgrass prairie region (Wilson and Ruff 1999).
Meadow voles prefer mesic grassland habitats and tend
to avoid woody vegetation (Getz 1985). They are primarily herbivores, eating grasses, sedges, and forbs
(Batzli 1985), but are also known to eat seeds, insects,
and fungi (Lindroth and Batzli 1984). Howe and Brown
(1999) recognized the impact of meadow vole herbivory
on plant communities. They found that voles reduced
forb biomass by 35 and 57% in high- and low-density
plantings of tallgrass prairie, and reduced forb diversity
by 4 and 25%, respectively. In a study in old-field
habitats, Ostfeld et al. (1997) found that meadow voles
avoided forested edges, as evidenced by lower predation
on tree seedlings on edges than \5 m into the field.
They concluded that the lower activity of voles has a
profound effect on the survival of tree propagules on
edges, and that the distribution of meadow voles relative to forest edges influences the composition and
distribution of plant species. Because of the potential
influence these small mammals may have on the composition and distribution of herbaceous communities,
Ostfeld and Canham (1993) suggest the population
dynamics of voles be viewed as a keystone process.
The potential effects of meadow voles on plant communities may be mediated by the palatability of individual plant species in the community. Mechanical and
chemical defensive strategies against herbivory help determine the palatability of plants. Mechanical defenses
such as pubescence, thorns, silica crystals in tissues, and
production of waxes or resins discourage or impede
plant herbivory (Fernandes 1994). Many plants contain
secondary metabolites such as terpenoids, nitrogen-containing compounds, and phenolics to serve as a chemical defense against herbivory (Crawley 1997). These
metabolites may be distasteful to herbivores, resulting
in a wide spectrum of relative palatabilities in plant
species. According to Fenner et al. (1999), the relative
palatability of plants in a grazed community is a key
determinant of the community’s species composition.
Ostfeld and Canham (1993) also felt that the palatability of tree seedlings played a role in the levels of
predation by voles observed in their study. Incorporating plant palatability into the broader question con526
cerning small mammal herbivory will strengthen our
understanding of voles’ effects on prairie plant
communities.
Our study investigated the impact of wooded edges
on meadow vole distributions in Iowa tallgrass prairie
reconstructions and the subsequent effects on native
prairie vegetation. Specifically, we examined 1) the distribution of meadow voles from wooded edges to
prairie interiors and 2) the patterns of herbivory by
meadow voles on relatively palatable and unpalatable
native seedlings as a function of distance from wooded
edges. We hypothesized that meadow voles would
avoid wooded edges and increase in abundance in
prairie interiors. Voles may avoid edges due to habitat
requirements (Manson et al. 1999) or if predation risk
is increased by predators using the edge (Lima and Dill
1990). This distributional gradient of meadow voles
would result in lower rates of herbivory on prairie
seedlings near the wooded edge. We expected both
palatable and unpalatable seedlings to show this response but anticipated that the magnitude of the response would vary. Herbivory on palatable seedlings
should be much higher than herbivory on unpalatable
seedlings at intermediate and far distances from the
edge. Experimental support of these hypotheses could
reveal the significance of wooded edges, not only on the
distribution of small mammals, but on the composition
and distribution of native prairie plants.
Methods
Study sites
Five reconstructed tallgrass prairie sites near Ames, IA
were targeted for study: Kurtz (42°7%N, 93°12%W), McFarland 1 (42°5%N, 93°34%W), McFarland 2 (42°6%N,
93°34%W), Ledges (41°59%N, 93°52%W), and Big Creek
(41°47%N, 93°44%W). Kurtz prairie was a 1.2 ha privately-owned, 6-year-old big bluestem/switchgrass (Andropogon gerardii/Panicum 6irgatum) prairie in
Marshall County, IA. McFarland 1 and 2 were located
at McFarland Park, a Story County Conservation Park
6 km northeast of Ames, IA. McFarland 1 was a 5.7
ha, 25-year-old, poor-quality switchgrass prairie with
large infestations of crown vetch (Coronilla 6aria). McFarland 2 was a 1.5 ha forb-rich, 5-year-old big
bluestem prairie. The 3.2 ha prairie at Ledges State
Park in Boone County, IA, was approximately 20 years
old and was dominated by switchgrass and reed canary
grass (Phalaris arundinacea). The final site was a 0.8 ha,
20-year-old big bluestem/switchgrass prairie at Big
Creek State Park in Polk County, IA.
Each prairie had a continuous wooded edge at least
100 m long. Kurtz, McFarland 2, and Big Creek had
south-facing edges, while McFarland 1 and Ledges had
east-facing edges. The trees of all the edges were apOIKOS 100:3 (2003)
proximately 10 m tall, but the thickness of the wooded
habitat varied from 2 to 30 m.
Determination of relative palatabilities
Laboratory trials of consumption of plants by meadow
voles were conducted from April through July 2000 to
determine which native prairie seedlings were palatable
and unpalatable for use in the field study. Plant species
tested included lead plant (Amorpha canescens Pursh),
indigobush amorpha (Amorpha fruticosa L.), wild blue
indigo (Baptisia australis [L.] R. Br.), prairie coreopsis
(Coreopsis palmata Nutt.), purple prairie clover (Dalea
purpurea Vent.), Illinois bundleflower (Desmanthus illinoensis [Michx.] MacM. ex B. L. Robinson & Fern.),
purple coneflower (Echinacea pallida [Nutt.] Nutt.),
alum root (Heuchera richardsonii R. Br.), blazing star
(Liatris aspera Michx.), and prairie violet (Viola pedatifida G. Don). These species were chosen for testing
because they are all common, endemic tallgrass prairie
forbs. In each trial, one native species was tested
against black medic (Medicago lupulina), a naturalized
forb native to Eurasia. Black medic has been shown to
be palatable to voles in previous trials (Danielson,
unpubl.), so it could be used to indicate the relative
palatability of native species. The placement of eight
seedlings of each species into a 4 × 4 tray was randomized by a latin square design. The tray consisted of 4
1204-size plastic inserts placed in a 19 × 19× 6 cm
plastic tray, and individuals were transplanted into a
cell of the insert. Meadow voles were live-trapped from
an area marsh and brought into the laboratory around
8 a.m. for a palatability trial. Individuals were each
placed in a 38 l aquarium containing sawdust bedding,
a 10 cm-diameter glass water dish, and a 10 × 12 cm
cardboard ‘‘tent’’ for hiding. Approximately 2 –5 hours
later, the tray of plants was placed in an aquarium with
a meadow vole for three hours. The percentage of each
species eaten was determined by scoring individual
plants as not eaten, half eaten, or entirely eaten. Voles
were then released into the field, so individuals were
only used once in the lab trials. Six trials on the
herbivory of each native species compared to black
medic were completed using a total of 60 voles.
10 m apart along the forest edge, as well as at distances
5, 10, 20, 30, and 40 m perpendicular to the edge. The
5 m distance was used to facilitate greater resolution of
small-mammal movement near the edge. Two Sherman
live traps were placed at each station, for a total of 60
live traps at 30 trap stations. To reduce any influence of
nearby edges, the grid was positioned so that there was
at least 30 m of open prairie on the 3 non-edge sides of
the grid. The traps were baited with oats and locked
open for 2 days, and then set for 5 days. Traps were
checked each morning of the 5 days; small mammals
were ear-tagged, sexed, and weighed, and traps were
re-set each afternoon. The trapping regime was repeated at all sites approximately 4 weeks after the
initial week of trapping. The dates of the second trapping session were 10 – 14 July 2000 for Kurtz, McFarland 1, and McFarland 2, and 24 – 28 July 2000 for
Ledges and Big Creek. Vole density was calculated by
averaging the minimum number of voles known alive
for the two trapping sessions at each site. Because the
area of each trapping grid was the same, the density is
expressed as the number of individual voles per site.
After one small-mammal trapping session was completed at all sites, experimental planting units were
established at each site within the 50 × 50 m trapping
grid. The experimental design consisted of four plots
spaced 10 m apart parallel to the forested edge, repeated at 2, 5, 10, 20, and 30 m from the edge, for a
total of 20 plots (Fig. 1). At each plot, approximately
Field methods
Small-mammals were trapped to determine the density
and distribution of meadow voles at each site. Because
of the distance between sites and time needed to check
traps, trapping occurred during two consecutive weeks:
12–16 June 2000 for Kurtz, McFarland 1 and McFarland 2, and 19 –23 June 2000 for Ledges and Big Creek.
Permanent trap stations were established in a 50 × 50 m
grid at each site (Fig. 1). Five trap stations were spaced
OIKOS 100:3 (2003)
Fig. 1. Design of small mammal trapping and herbivory experiment at five reconstructed prairie sites in central Iowa. ‘x’
represents location of a Sherman live trap. The boxes represent
the location of a mound on which seedlings were transplanted.
Each square represents a different plant species and each circle
represents an individual plant.
527
7.5 l of topsoil were deposited on the ground to simulate a pocket gopher (Geomys bursarius) mound. The
mounds serve as small-scale disturbances which provide
opportunities for forb colonization (Peart 1989, WolfeBellin and Moloney 2000). In this study, mounds created homogeneous microhabitats for planting seedlings
and provided a realistic condition for the presence of
numerous forb seedlings. Mounds also helped to eliminate other environmental effects that may be connected
with distance from edges (e.g. moisture, plant density,
light availability, etc.). On each mound, nine plants
each of a palatable species and an unpalatable species
were planted approximately one inch apart in an array
(Fig. 1). Based on the laboratory trials and the desire to
use leguminous species that are easy to grow, purple
prairie clover (Dalea purpurea) was used as the relatively palatable species, and Illinois bundleflower (Desmanthus illinoensis) as the relatively unpalatable species
(see Results). Each species was planted in a 3 × 3 array,
the two arrays were adjacent to one another, and the
position of the species (right or left side of the array)
was randomized. Purple prairie clover and Illinois bundleflower were planted at four sites in this manner, but
due to an insufficient number of Illinois bundleflower
seedlings, lead plant (Amorpha canescens) was substituted as the unpalatable species at the fifth site (Kurtz).
Initial palatability trials indicate Illinois bundleflower
and lead plant are both relatively unpalatable to voles
(see Results), but statistical analyses for the unpalatable
species did not include lead plant. Seedlings were transplanted onto the mounds 18–20 July 2000. Because
herbivory at the seedling stage results in the death of
individual plants, we recorded herbivory as the number
of stems clipped per species per plot 1 week and 4
weeks after planting.
Results
Fig. 2. The within-site proportion of vole captures at six
distances from the wooded edge for high vole-density sites (a)
and low vole-density sites (b) over two trapping sessions
(dotted line =site not used in unpalatable species analyses).
Live-trapping indicated that meadow voles were less
abundant at the edge and increased toward the prairie
interior (ANOVA, p=0.037). The proportion of voles
captured along the edge was very low for all sites, and
at three high vole-density sites (22 –49.5 mean MNA),
the proportion of captures generally increased with
increasing distance from the edge (Fig. 2a). At the
remaining two sites, this pattern was not as apparent
because of low vole densities (5.5 –8.5 mean MNA), but
even so, fewer voles were captured at the edge (Fig. 2b).
While there was a definite edge effect, the response by
voles to the edge was not linear, nor was the edge effect
very wide.
Laboratory trials revealed that five native species
were significantly less palatable than our standard forage plant, Medicago lupulina, using paired t-tests (Table
1). Prior to statistical tests, the data were arcsine
square-root transformed. The percent herbivory was
significantly greater on Medicago lupulina than on each
of the native species Amorpha canescens, A. fruticosa,
Desmanthus illinoensis, Heuchera richardsonii, and Viola
pedatifida (p B0.05), which we hereafter refer to as
‘‘unpalatable’’. The remaining five native species are
relatively palatable, since there was not a statistically
significant difference in the percent herbivory of these
five natives versus Medicago lupulina. The two species
chosen for use in the field study, Dalea purpurea and
Desmanthus illinoensis, were among the most palatable
and least palatable according to our tests.
Despite laboratory trials indicating that Desmanthus
illinoensis was less palatable than Dalea purpurea, there
was no significant difference in the number of unpalatable versus palatable plants eaten in the field (t-test on
528
OIKOS 100:3 (2003)
Table 1. Paired t-tests compare the amount of herbivory of 10 species of native tallgrass prairie plants versus herbivory of
Medicago lupulina in laboratory trials. Significant values (pB0.05, *) indicate the native species that were eaten significantly less
than M. lupulina, and were therefore classified as relatively ‘‘unpalatable’’. No plant was eaten significantly more often than M.
lupulina. The maximum mean difference in herbivory of M. lupulina versus each native species is 8 plants.
Species
Mean difference in
herbivory Medicago – native
SD of difference
Relative Palatability
Amorpha canescens
Amorpha fruticosa
Baptisia australis
Coreopsis palmata
Dalea purpurea
Desmanthus illinoensis
Echinacea pallida
Heuchera richardsonii
Liatris aspera
Viola pedatifida
2.0*
4.17*
2.08
0.25
0.67
4.92*
2.58
3.08*
1.25
3.0*
2.17
3.14
2.50
0.42
1.63
2.56
3.48
2.54
1.97
2.51
unpalatable
unpalatable
palatable
palatable
palatable
unpalatable
palatable
unpalatable
palatable
unpalatable
difference, p =0.33 after 1 week, p =0.12 after 4
weeks). There was, however, a significant difference in
the percentage of plants eaten at different distances
from the edge (Fig. 3a and b). A 2-way analysis of
variance (ANOVA) was used to analyze the effects of
site, distance, and the site-distance interaction on the
amount of herbivory of relatively palatable and unpalatable species after 1 week and 4 weeks (SAS v. 8.1;
Table 2). Distance had a significant effect on herbivory
of less palatable plants after 1 week (p = 0.002), and a
marginally insignificant effect after 4 weeks (p = 0.08).
Distance also had a significant effect on herbivory of
the more palatable plants after both 1 week and 4
weeks (pB0.0001 for both time intervals). Fig. 3 indicates that both species of plants were eaten less at 2 m
from the edge than the other distances. This difference
between 2 m and the other distances is significant
except for the relatively unpalatable species at 4 weeks
(p B0.01 using Scheffe’s multiple comparisons adjustment for any possible contrast).
Although seedlings in the field were susceptible to
herbivory by other herbivores such as deer and rabbits,
we are confident the herbivory we observed was primarily due to meadow voles. Deer were occasionally observed in the vicinity of the sites, but not in the grids,
and rabbits were never observed at any of the sites. An
abundance of meadow vole fecal material on the
mounds also indicated plants were not eaten by other
herbivores. Even if deer and rabbits were active on the
sites, we would expect herbivory patterns opposite of
our observations. Meiners and Martinkovic (2002)
found that herbivory of red oak tree seedings by both
deer and rabbits decreased significantly from forest
interiors to old-field interiors. Had these mammals been
depredating the seedlings in our study, we would likely
have observed more herbivory at the wooded edge
instead of less.
The percent herbivory of the more palatable species
varied significantly by site after both 1 and 4 weeks,
and after 1 week for the less palatable species (Table 2).
Part of the difference in herbivory among sites was
OIKOS 100:3 (2003)
Fig. 3. Mean percent herbivory of unpalatable and palatable
seedlings after a) one week, and b) four weeks as a function of
distance from the wooded edge.
529
Table 2. Summary statistics of the ANOVA model examining the effects of site and distance on the amount of herbivory of
relatively unpalatable and palatable species after 1 week and 4 weeks.
Source of variation
ss
df
F
p
Source of variation
Unpalatable species
ss
df
F
p
Palatable species
1 week
site
Distance
site×distance
error
total
4 weeks
site
Distance
site×distance
error
total
86.16
134.27
126.81
415.75
762.99
3
4
12
60
79
4.14
4.84
1.53
0.0098
0.0019
0.1404
site
distance
site×distance
error
total
145.22
259.42
144.71
447.75
997.10
4
4
16
75
99
6.08
10.86
1.51
0.0003
0.0001
0.1169
3.01
18.39
26.08
126.00
173.48
3
4
12
60
79
0.48
2.19
1.03
0.6987
0.0809
0.4300
site
distance
site×distance
error
total
112.09
100.84
58.52
235.63
507.08
4
4
16
75
99
8.92
8.02
1.16
0.0001
0.0001
0.3162
related to the average vole density. A linear contrast on
the portion of site variance attributable to vole density
was estimated in the ANOVA model. A linear contrast
in an ANOVA model partitions the variance of a main
effect into a linear component and leftover variance,
and tests whether the linear component explains a
statistically significant portion of the main effect variance (Ramsey and Schafer 1997). The linear contrast
for vole density was significant for the more palatable
species at both time intervals (p = 0.0027 and 0.004,
respectively), and for the less palatable species after 1
week (p = 0.048). This indicates that vole density explained a statistically significant portion of the variance
in herbivory by site. The pattern of increased herbivory
with increasing vole density was strongest after 1 week,
although after 4 weeks, there was still less herbivory at
low-density sites than medium to high-density sites
(Table 3).
Discussion
Wooded edges had an effect on meadow vole distribution and native prairie seedling herbivory in Iowa tallgrass prairie reconstructions, as predicted. Meadow
voles were less abundant at the wooded edge than all
other distances toward the prairie interior. Comparing
high vole-density sites (Fig. 2a) to low vole-density sites
(Fig. 2b), it appears that wooded edges play a role in
the way in which meadow voles fill habitats. At low
densities, voles are found in low numbers at all distances except the edge, where they are almost absent.
As vole numbers increase, however, the proportion of
voles found in the prairie interior increases greatly
while the proportion found at and near the edge remains low. Voles seem to preferentially occupy habitat
that is far from the wooded edge ( \10 m). Two
probable causes for this pattern are microhabitat
changes and an increased risk of predation near the
edge. Meadow voles are strictly grassland dwellers;
rarely do they enter forested habitats (Wilson and Ruff
1999). Because the habitat changed abruptly from
grassland to woody vegetation in our study, it is not
surprising that we found few voles at the wooded edge,
but considerably more as close as 5 – 10 m from the
edge.
Predation pressure also may contribute to the observed distribution pattern. Predators of meadow voles
include raptors like owls and hawks, and a variety of
mammals such as fox, opossum, raccoon, skunk, badger, weasel, mink, and coyotes (Pearson 1985). Most of
these predators are thought to use wooded edges as
Table 3. Mean Minimum number known alive density of voles per site and mean percent herbivory of unpalatable species and
palatable species after one and four weeks for each site. Standard deviation of the mean percent herbivory is in parentheses.
*Lead plant is the unpalatable species at Kurtz; Illinois bundleflower is the unpalatable species at the other sites.
Site
Mean Vole Density
Mean % Herbivory
1 week
Kurtz*
McFarland 2
Big Creek
McFarland 1
Ledges
530
5.5
8.5
22.5
28.0
49.5
4 weeks
unpalatable
palatable
unpalatable
palatable
55.8
57.5
80.3
88.9
78.3
51.7
55.0
82.5
83.3
72.5
70.0
95.0
99.2
93.6
95.8
65.8
88.6
100.0
87.8
95.6
(1.58)
(0.95)
(1.72)
(2.10)
(2.84)
(1.52)
(0.99)
(1.58)
(2.83)
(3.39)
(1.67)
(0.64)
(0.15)
(1.29)
(0.84)
(1.35)
(1.14)
(0.00)
(2.46)
(0.89)
OIKOS 100:3 (2003)
perches while searching for prey or as corridors for
travel (Marini et al. 1995), although direct evidence of
increased predation along wooded edges has been
difficult to obtain (Heske 1995, Heske et al. 1999).
Winter et al. (2000) found the activity of mid-sized
mammalian grassland nest predators tended to increase
with increasing proximity to wooded edges, which suggests that voles may avoid edges to reduce the risk of
predation. In a study on Tengmalm’s owls (Aegolius
funereus) in Norway, Jacobsen and Sonerud (1993)
found that the amount of ground vegetation influenced
where the owls hunt. These owls employ a pause-travel
mode of hunting in which they perch in trees to locate
their prey auditorily. When the ground became snowfree in early spring, the owls hunted more in clear-cuts,
but when the ground vegetation of the clear-cuts became denser in late spring, they switched to hunting in
the forest. This suggests that it may be difficult for
raptors to find prey items in grassland vegetation that is
far from the edge. Sonerud (1992) also reported that for
hawk owls (Surnia ulula), which hunt similarly to Tengmalm’s owls, shorter attack distances from the perch
were more successful. Both of these studies suggest why
the edge effect in our study was present, but not very
wide.
Even though the zone of influence of the wooded
edge on vole distribution is narrow, it is biologically
important. Both the relatively palatable and unpalatable plant species were eaten less at 2 m from the edge
than at the other distances (Fig. 3). We believe that
edges may therefore provide a small, yet important,
refuge for native seedling establishment. After 4 weeks
in the field, 92 –100% of all seedlings at 5 –30 m distances from the edge had been eaten, whereas 66% of
the more palatable and 86% of the less palatable
seedlings were eaten at 2 m from the edge (Fig. 3b).
Because voles avoid edges, the risk of herbivory is
reduced, and seedlings have a greater chance of establishment near wooded edges. Consequently, wooded
edges may be beneficial to prairie plant species, especially those species that rely more heavily on seedling
recruitment for continued existence.
The length of time that wooded edges serve as a
refuge for prairie plants is unclear, and may vary
depending on the nature of the wooded edge and
prairie management practices. If tree seedlings begin to
invade the prairie, the habitat will become degraded
and edges will have an overall negative impact on
prairie plants. Voles may be able to prevent invasion at
further distances from the edge by their herbivory on
tree seedlings, but may not be able to fully stop invasion near the edge (Ostfeld et al. 1997). In our study,
however, ‘‘hedgerow’’-type edges did not appear to be
invasive, and invasion from thicker woods could be
prevented with standard prairie management such as
cutting brush and burning. Prairie seedlings, therefore,
OIKOS 100:3 (2003)
should still enjoy at least a temporary refuge along
wooded edges, and with management to prevent woody
invasion, the duration of the refuge could be prolonged.
Seemingly, native prairie seedlings may never become
established in prairie interiors due to the high rates of
herbivory by meadow voles. However, vole populations
are well-known for their dramatic temporal variationpopulations are not maintained at high densities for
long periods of time (Krebs and Myers 1974, Taitt and
Krebs 1985, Getz et al. 1987, Getz and Hofmann 1999).
We found that vole density explained a significant
portion of the variance in herbivory by site, with less
herbivory at low vole-density sites and greater herbivory at high vole-density sites (Table 3). During
periods of high density, prairie seedlings may indeed be
unable to survive in prairie interiors due to the high
rates of herbivory. But in low vole-density periods,
seedlings may have a chance to escape herbivory and
survive, even in prairie interiors. These findings are
consistent with other research showing that small-mammal herbivores at high densities affect plant communities (Brown and Heske 1990, Bergeron and Jodoin
1993, Ostfeld and Canham 1993).
The most surprising result of this study was the lack
of a difference in depredation of relatively palatable
and unpalatable seedlings in the field. The laboratory
trials indicated clear differences in the palatability of
several species, but in the field, the amount of herbivory
on relatively palatable and unpalatable seedlings was
not statistically different. Seasonal differences between
when the lab study and field study were conducted may
account for this phenomenon. Laboratory trials for the
species used in the field were performed from late April
to mid June, but the herbivory experiment did not
begin until late July. Meadow voles brought into the
lab earlier in the season may have been satiated and
could therefore afford to discern between palatable and
unpalatable species. By late July, voles in the field may
have been experiencing shortages of preferred green
shoots, restricting them from the luxury of choosing
between species. In fact, any seedling at this time of the
year may be ‘‘relatively palatable’’ and worth eating
because of the scarcity of seedlings in the habitat.
An alternative explanation lies in the observation
that some plants scored as depredated were clipped but
not eaten. The number of mounds on which clipped
seedlings of either species occurred was noted, but
unfortunately, the number of individual plants that
were clipped was not recorded. Uneaten clippings of
Illinois bundleflower, a less palatable species, were
found on 28 of 80 mounds, while clippings of purple
prairie clover, the relatively palatable species, were
found significantly less on 3 of 80 mounds (x2 = 25.0,
p B 0.005). Although clipping is the same as herbivory
from the plant’s point of view, voles may have found
531
Illinois bundleflower distasteful only after sampling
them, resulting in the appearance of not distinguishing
between relatively palatable and unpalatable species. In
the field, voles may not take the time to choose between
palatable and unpalatable species until after they have
sampled them due to predation risk.
While the clipping behavior is most likely due to
sampling plants, meadow voles may also use clipping as
a means of modifying their environment. Meadow voles
depredated tree seedlings in Ostfeld and Canham’s
(1993) study, but this was not viewed as having a
functional role in their nutrition since the trees were not
eaten. As tree seedlings invade grassland habitat, habitat quality diminishes, so the clipping of tree seedlings
by voles may be a mechanism for maintaining preferred
habitat. A similar behavior may have occurred in our
study, whereby voles use clipping as a means to remove
distasteful species from their environment. Future research on this question is warranted and could reveal
some intriguing vole-plant interactions.
We have demonstrated that wooded edges along
tallgrass prairie reconstructions influence both the
small-mammal and plant communities. Meadow vole
abundance changes with respect to wooded edges and
vole herbivory on native prairie seedlings is reduced at
the edge. This results in a small area of refuge for
seedlings near wooded edges. Meadow voles undoubtedly impact the distribution of native forbs in prairie
ecosystems through their own distribution, population
density, and perhaps behavior. That wooded edges are
capable of changing the interaction between voles and
prairie plants is of great consequence in our overall
understanding of how prairies function in such a fragmented ecosystem.
Acknowledgements – We thank Kelly Wolfe-Bellin for her help
in designing and completing the lab palatability trials, as well
as her immeasurable aid to the primary author throughout the
study. Lisa Young provided field assistance and Philip Dixon
was helpful with the statistical analyses. We also thank the
following people for their permission to work at the study sites
and their provision of site background information: Carl
Kurtz, Steve Lekwa (Story County Conservation, McFarland
Park), Mark Peter (State Preserves Board, Ledges State Park),
and Kim Olofson (State Preserves Board, Big Creek State
Park).
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